Abstract
Considerable progress in our understanding of long-distance migration has been achieved thanks to the use of small geolocator devices (GLS). The tracking of resident or short-distance migrant animals remains however challenging because geolocation errors are substantial and difficult to estimate. This study aims to examine the sex-specific marine space uses of a resident tropical seabird, the masked booby (Sula dactylatra), during its full annual life cycle at the Fernando de Noronha archipelago (Brazil). Masked boobies (n = 31) tagged with GLS recording light intensity, seawater immersion, and water temperature showed a resident behaviour over their entire annual cycle. A wavelet analysis of GLS data revealed oscillatory patterns of inferred longitude correlated with changes in immersion frequency. This synchronicity demonstrated that birds traveled away and back from the colony on consecutive trips of short length (\(\sim\) 2–4 days) and short range (\(\sim\) 100–300 km) eastward of the colony. Duration and range of trips depended on the sex of the individual and on the time of the year. Trip duration increased gradually from the end of the breeding period to the post-breeding period, probably due to the release of the central-place breeding constraints. During the pre-breeding period, females had farther ranges eastward and spent more time in water than males. Despite inherent limits of light-based geolocation, this study demonstrates the relevance of synchronicity analysis of GLS data for investigating year-round movements of resident or short-distance migrants.
Similar content being viewed by others
Data/Code availability
Data and code are available on our github page: https://github.com/AmedeeRoy/WaveLightGLS.
References
Antas PTZ (1991) Status and conservation of seabirds breeding in Brazilian waters. ICBP Tech Publ 11:141–158
Ashmole N (1971) Seabird ecology and the marine environment. Avian Biol 1:223–286
Bächler E, Hahn S, Schaub M, Arlettaz R, Jenni L, Fox JW, Afanasyev V, Liechti F (2010) Year-round tracking of small trans-Saharan migrants using light-level geolocators. PLoS One 5:e9566. https://doi.org/10.1371/journal.pone.0009566
Ballance LT, Pitman RL, Fiedler PC (2006) Oceanographic influences on seabirds and cetaceans of the eastern tropical Pacific: a review. Prog Oceanogr 69:360–390. https://doi.org/10.1016/j.pocean.2006.03.013
Bertrand A, Gerlotto F, Bertrand S, Gutiérrez M, Alza L, Chipollini A, Díaz E, Espinoza P, Ledesma J, Quesquén R, Peraltilla S, Chavez F (2008) Schooling behaviour and environmental forcing in relation to anchoveta distribution: an analysis across multiple spatial scales. Prog Oceanogr 79:264–277. https://doi.org/10.1016/j.pocean.2008.10.018
Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225. https://doi.org/10.1017/S1464793104006645
Cazelles B, Stone L (2003) Detection of imperfect population synchrony in an uncertain world. J Anim Ecol 72:231–242. https://doi.org/10.1046/j.1365-2656.2003.00763.x
Cazelles B, Chavez M, Berteaux D, Ménard F, Vik JO, Jenouvrier S, Stenseth NC (2008) Wavelet analysis of ecological time series. Oecologia 156:287–304. https://doi.org/10.1007/s00442-008-0993-2
Cazelles B, Cazelles K, Chavez M (2014) Wavelet analysis in ecology and epidemiology: impact of statistical tests. J R Soc Interface 11:20130585. https://doi.org/10.1098/rsif.2013.0585
Clayson CA, Weitlich D (2007) Variability of tropical diurnal sea surface temperature. J Clim 20:334–352. https://doi.org/10.1175/JCLI3999.1
Campelo RPS, Bonou FK, de Melo Júnior M, Diaz XFG, Bezerra LEA, Neumann-Leitão S (2019) Zooplankton biomass around marine protected islands in the tropical Atlantic Ocean. J Sea Res 154:101810. https://doi.org/10.1016/j.seares.2019.101810
Del Hoyo J, Elliott A, Sargatal J (1992) Handbook of the birds of the world, vol 1. Lynx Editions, Barcelona
Diamond AW (1978) Feeding strategies and population size in tropical seabirds. Am Nat 112:215–223
Egevang C, Stenhouse IJ, Phillips RA, Petersen A, Fox JW, Silk JRD (2010) Tracking of Arctic terns Sterna paradisaea reveals longest animal migration. Proc Natl Acad Sci 107:2078–2081. https://doi.org/10.1073/pnas.0909493107
Ekstrom P (2007) Error measures for template-fit geolocation based on light. Deep Sea Res Part II Top Stud Oceanogr 54:392–403. https://doi.org/10.1016/j.dsr2.2006.12.002
Fablet R, Chaigneau A, Bertrand S (2013) Multiscale analysis of geometric planar deformations: application to wild animal electronic tracking and satellite ocean observation data. IEEE Trans Geosci Remote Sens 52:3627–3636. https://doi.org/10.1109/TGRS.2013.2274157
Friesen VL, Burg TM, McCOY KD (2007) Mechanisms of population differentiation in seabirds. Mol Ecol 16:1765–1785. https://doi.org/10.1111/j.1365-294X.2006.03197.x
Garthe S, Ludynia K, Hüppop O, Kubetzki U, Meraz JF, Furness RW (2012) Energy budgets reveal equal benefits of varied migration strategies in northern gannets. Mar Biol 159:1907–1915. https://doi.org/10.1007/s00227-012-1978-6
González-Solís J, Croxall JP, Oro D, Ruiz X (2007) Trans-equatorial migration and mixing in the wintering areas of a pelagic seabird. Front Ecol Environ 5:297–301. https://doi.org/10.1890/1540-9295(2007)5[297:TMAMIT]2.0.CO;2
Guilford T, Meade J, Willis J, Phillips R, Boyle D, Roberts S, Collett M, Freeman R, Perrins C (2009) Migration and stopover in a small pelagic seabird, the Manx shearwater Puffinus puffinus: insights from machine learning. Proc R Soc Lond B Biol Sci 276:1215–1223. https://doi.org/10.1098/rspb.2008.1577
Hill RD (1994) Theory of geolocation by light levels. In: Le Boeuf BJ, Laws RM (eds) Elephant seals: population ecology, and physiology. University of California Press, Berkeley, pp 227–236
Jaquemet S, Le Corre M, Weimerskirch H (2004) Seabird community structure in a coastal tropical environment: importance of natural factors and fish aggregating devices (FADs). Mar Ecol Prog Ser 268:281–292
Jenouvrier S, Weimerskirch H, Barbraud C, Park YH, Cazelles B (2005) Evidence of a shift in the cyclicity of Antarctic seabird dynamics linked to climate. Proc R Soc Lond B Biol Sci 272:887–895. https://doi.org/10.1098/rspb.2004.2978
Kepler CB (1969) The breeding biology of the blue-faced booby (Sula dactylatra personata) on Green Island, Kure atoll. Publications of the Nuttall Ornithologists Club, p 8
Leal GR, Furness RW, McGill RAR, Santos RA, Bugoni L (2017) Feeding and foraging ecology of Trindade petrels Pterodroma arminjoniana during the breeding period in the South Atlantic Ocean. Mar Biol 164:211. https://doi.org/10.1007/s00227-017-3240-8
Lerma M, Serratosa J, Luna-Jorquera G, Garthe S (2020) Foraging ecology of masked boobies (Sula dactylatra) in the world’s largest “oceanic desert”. Mar Biol 167:87. https://doi.org/10.1007/s00227-020-03700-2
Lewis S, Schreiber EA, Daunt F, Schenk GA, Orr K, Adams A, Wanless S, Hamer KC (2005) Sex-specific foraging behaviour in tropical boobies: does size matter? Ibis 147:408–414. https://doi.org/10.1111/j.1474-919x.2005.00428.x
Lisovski S, Hewson CM, Klaassen RHG, Korner-Nievergelt F, Kristensen MW, Hahn S (2012) Geolocation by light: accuracy and precision affected by environmental factors. Methods Ecol Evol 3:603–612. https://doi.org/10.1111/j.2041-210X.2012.00185.x
Lisovski S, Wotherspoon S, Sumner M (2016) TwGeos: basic data processing for light-level geolocation archival tags. R package version 0.1.2. https://github.com/slisovski/TwGeos
Lisovski S, Schmaljohann H, Bridge ES, Bauer S, Farnsworth A, Gauthreaux SA, Hahn S, Hallworth MT, Hewson CM, Kelly JF, Liechti F, Marra PP, Rakhimberdiev E, Ross JD, Seavy NE, Sumner MD, Taylor CM, Winkler DW, Wotherspoon SJ, Wunder MB (2018) Inherent limits of light-level geolocation may lead to over-interpretation. Curr Biol 28:R99–R100. https://doi.org/10.1016/j.cub.2017.11.072
Lisovski S, Bauer S, Briedis M, Davidson SC, Dhanjal-Adams KL, Hallworth MT, Karagicheva J, Meier CM, Merkel B, Ouwehand J, Pedersen L, Rakhimberdiev E, Roberto-Charron A, Seavy NE, Sumner MD, Taylor CM, Wotherspoon SJ, Bridge ES (2019) Light-level geolocator analyses: a user’s guide. J Anim Ecol 89:221–236. https://doi.org/10.1111/1365-2656.13036
Longhurst AR, Pauly D (1987) Ecology of tropical oceans. Academic Press, San Diego (574.52636 L6)
Mancini PL, Bond AL, Hobson KA, Duarte LS, Bugoni L (2013) Foraging segregation in tropical and polar seabirds: testing the intersexual competition hypothesis. J Exp Mar Biol Ecol 449:186–193. https://doi.org/10.1016/j.jembe.2013.09.011
Mancini PL, Hobson KA, Bugoni L (2014) Role of body size in shaping the trophic structure of tropical seabird communities. Mar Ecol Prog Ser 497:243–257. https://doi.org/10.3354/meps10589
Mancini PL, Serafini PP, Bugoni L (2016) Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization. Rev Brasil Ornitol 24:94–115. https://doi.org/10.1007/BF03544338
Merkel B, Phillips RA, Descamps S, Yoccoz NG, Moe B, Strøm H (2016) A probabilistic algorithm to process geolocation data. Mov Ecol 4:26. https://doi.org/10.1186/s40462-016-0091-8
Nathan R, Getz WM, Revilla E, Holyoak M, Kadmon R, Saltz D, Smouse PE (2008) A movement ecology paradigm for unifying organismal movement research. Proc Natl Acad Sci USA 105:19052–19059. https://doi.org/10.1073/pnas.0800375105
Nelson B (2005) Pelicans, cormorants, and their relatives: the Pelecaniformes. Oxford University Press, Oxford
Newton I (2008) The migration ecology of birds. Academic Press, London
Nunes GT, Bertrand S, Bugoni L (2018) Seabirds fighting for land: phenotypic consequences of breeding area constraints at a small remote archipelago. Sci Rep 8:665. https://doi.org/10.1038/s41598-017-18808-7
Olson PA, Ballance LT, Hough KR, Dutton PH, Reilly SB (2001) Summary of seabird, marine turtle, and surface fauna data collected during a survey in the eastern tropical pacific ocean July 8–December 9, 2000. NOAA Techn Memo NMFS NOAA-TM-NMFS-SWFSC-304
Phillips R, Silk J, Croxall J, Afanasyev V, Briggs D (2004) Accuracy of geolocation estimates for flying seabirds. Mar Ecol Prog Ser 266:265–272. https://doi.org/10.3354/meps266265
Poli CL, Harrison AL, Vallarino A, Gerard PD, Jodice PGR (2017) Dynamic oceanography determines fine scale foraging behavior of masked boobies in the Gulf of Mexico. PLoS One 12:18. https://doi.org/10.1371/journal.pone.0178318
Pollet IL, Hedd A, Taylor PD, Montevecchi WA, Shutler D (2014) Migratory movements and wintering areas of Leachs storm-petrels tracked using geolocators. J Field Ornithol 85:321–328. https://doi.org/10.1111/jofo.12071
Ropert-Coudert Y, Wilson RP, Daunt F, Kato A (2004) Patterns of energy acquisition by a central place forager: benefits of alternating short and long foraging trips. Behav Ecol 15:824–830. https://doi.org/10.1093/beheco/arh086
Rosch A, Schmidbauer H (2018) WaveletComp R package version 1.1. https://cran.r-project.org/package=WaveletComp
Rouyer T, Fromentin JM, Stenseth NC, Cazelles B (2008) Analysing multiple time series and extending significance testing in wavelet analysis. Mar Ecol Prog Ser 359:11–23. https://doi.org/10.3354/meps07330
Sazima I, de Almeida LB (2008) The bird kraken: octopus preys on a sea bird at an oceanic island in the tropical West Atlantic. Mar Biodivers Rec 1:e47. https://doi.org/10.1017/S1755267206005458
Schacter CR, Jones IL (2018) Confirmed year-round residence and land roosting of whiskered auklets (Aethia pygmaea) at Buldir Island, Alaska. Auk 135:706–715. https://doi.org/10.1642/AUK-17-235.1
Serrano-Meneses MA, Székely T (2006) Sexual size dimorphism in seabirds: sexual selection, fecundity selection and differential niche-utilisation. Oikos 113:385–394. https://doi.org/10.1111/j.0030-1299.2006.14246.x
Shaffer SA, Tremblay Y, Weimerskirch H, Scott D, Thompson DR, Sagar PM, Moller H, Taylor GA, Foley DG, Block BA, Costa DP (2006) Migratory shearwaters integrate oceanic resources across the Pacific Ocean in an endless summer. Proc Natl Acad Sci USA 103:12799–12802. https://doi.org/10.1073/pnas.0603715103
Sommerfeld J, Kato A, Ropert-Coudert Y, Garthe S, Hindell MA (2013) Foraging parameters influencing the detection and interpretation of area-restricted search behaviour in marine predators: a case study with the masked booby. PLoS One 8:e63742. https://doi.org/10.1371/journal.pone.0063742
Stenhouse IJ, Egevang C, Phillips RA (2012) Trans-equatorial migration, staging sites and wintering area of Sabine’s gulls Larus sabini in the Atlantic Ocean. Ibis 154:42–51. https://doi.org/10.1111/j.1474-919X.2011.01180.x
Torrence C, Compo GP (1998) A practical guide to wavelet analysis. Bull Am Meteorol Soc 79:61–78
Wakefield E, Phillips R, Matthiopoulos J (2009) Quantifying habitat use and preferences of pelagic seabirds using individual movement data: a review. Mar Ecol Prog Ser 391:165–182. https://doi.org/10.3354/meps08203
Weimerskirch H, Wilson RP (2000) Oceanic respite for wandering albatrosses. Nature 406:955–956. https://doi.org/10.1038/35023068
Weimerskirch H, Le Corre M, Gadenne H, Pinaud D, Kato A, Ropert-Coudert Y, Bost CA (2009) Relationship between reversed sexual dimorphism, breeding investment and foraging ecology in a pelagic seabird, the masked booby. Oecologia 161:637–649. https://doi.org/10.1007/s00442-009-1397-7
Wilkinson BP, Haynes-Sutton AM, Meggs L, Jodice PGR (2020) High spatial fidelity among foraging trips of masked boobies from Pedro Cays, Jamaica. PLoS One 15:e0231654. https://doi.org/10.1371/journal.pone.0231654
Wilson RP, Culik BM, Kosiorek P, Adelung D (1998) The over-winter movements of a chinstrap penguin (Pygoscelis antarctica). Polar Rec 34:107–112. https://doi.org/10.1017/S0032247400015242
Wilson R, Grémillet D, Syder J, Kierspel M, Garthe S, Weimerskirch H, Schäfer-Neth C, Scolaro J, Bost C, Plötz J, Nel D (2002) Remote-sensing systems and seabirds: their use, abuse and potential for measuring marine environmental variables. Mar Ecol Prog Ser 228:241–261. https://doi.org/10.3354/meps228241
Woodward PW (1972) The natural history of Kure Atoll, northwestern Hawaiian islands. Atoll Res Bull 164:1-317. https://doi.org/10.5479/si.00775630.164.1
Wotherspoon SJ, Sumner MD, Lisovski S (2016) SGAT: solar/satellite geolocation for animal tracking. R package version 0.1.3. https://github.com/SWotherspoon/SGAT
Young H, Shaffer S, McCauley D, Foley D, Dirzo R, Block B (2010) Resource partitioning by species but not sex in sympatric boobies in the central Pacific Ocean. Mar Ecol Prog Ser 403:291–301. https://doi.org/10.3354/meps08478
Acknowledgements
We would like to thank all people involved in the fieldwork activities. Fieldwork activities received the administrative and logistical support from the Fernando de Noronha administration, the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio, Brazil), the military firemen from Fernando de Noronha and the TAMAR Project. We also want to express grateful thanks to anonymous reviewers and to colleagues from IFREMER and IRD for having helped us significantly on the manuscript.
Funding
This work is a contribution to the TRIATLAS project (funding by the European Union’s Horizon 2020 research and innovation program—Grant agreement No. 817578). This project has received funding from the Paddle Rise project—European Union’s Horizon 2020 research and innovation program under Grant Agreement No. 734271. This study was partially funded by IRD (Mixed International Laboratory Tapioca), CPER Celimer (France), Fundação O Boticário (Brazil), Young Team IRD Programm Tabasco (JEAI) and Brazilian National Research Council (CNPq, No. 422759/2016-3). L.B. is research fellow from CNPq (PQ 311409/2018-0).
Author information
Authors and Affiliations
Contributions
AR, SB and KD conceived the ideas and AR performed the analysis; AR, GT, KD, CB, KD and SB have been on fieldworks for collecting the data; AR led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
This work was conducted with the approval of the Brazilian Ministry of Environment—Instituto Chico Mendes de Conservação da Biodiversidade (Authorization No 52583-5).
Additional information
Reviewers: undisclosed experts.
Responsible Editor: V. Paiva.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Roy, A., Delord, K., Nunes, G.T. et al. Did the animal move? A cross-wavelet approach to geolocation data reveals year-round whereabouts of a resident seabird. Mar Biol 168, 114 (2021). https://doi.org/10.1007/s00227-021-03923-x
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-021-03923-x